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Ocean temperature, but not acidification, causes sea anemone bleaching under a near-future climate scenario

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Abstract

Climate change is causing ocean temperature and partial pressure of carbon dioxide (pCO2) to increase. For sea anemones that have Symbiodiniaceae, high temperatures induce bleaching, whereas rises in pCO2 can enhance photosynthesis and increase host growth and abundance. It is, however, not clear how the interaction of these two stressors impacts sea anemones that provide habitat for anemonefishes. Here, we investigated the bleaching response of the sea anemone Entacmaea quadricolor, under four conditions: (i) current temperature and current pCO2 (control); (ii) future pCO2; (iii) future temperature; and (iv) future temperature and future pCO2. After 16 days of exposure, future temperature, but not pCO2 nor their interaction, significantly reduced the Symbiodiniaceae density and total chlorophyll Symbiodiniaceae cell−1. Colour score was lower in the sea anemones exposed to future temperature than current temperature from day 4 onwards. In contrast, total chlorophyll symbiont cell−1 increased in the future temperature treatments, and light-adapted effective quantum yield remained similar in all treatments. Although pCO2 had no impact within the time frame of our experiment, the predicted future temperature induced bleaching in E. quadricolor. As bleaching events increase in frequency and severity, this will likely impact the abundance of host sea anemones and their symbiotic anemonefishes.

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References

  • Alshwairikh Y (2018) A comparative assessment of the physiological performance of red sea and non-red sea symbiodiniaceae strains in acute heat and light-stress conditions. Doctoral dissertation, King Abdullah University of Science and Technology

  • Allemand D, Furla P, Bénazet-Tambutté S (1998) Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Canadian Journal of Botany 76:925–941

  • American Public Health Association (2005) Standard methods for the examination of water and wastewater. American Public Health Association (APHA): Washington, DC, USA

  • Anthony KR, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proceedings of the National Academy of Sciences 105(45):17442–17446

  • AOAC (2000) Official methods of analysis of AOAC International. Association of Official Analytical Chemists, Rockville, USA

  • Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annual Review of Ecology, Evolution, and Systematics 34:661–689

  • Beldade R, Blandin A, O’Donnell R, Mills SC (2017) Cascading effects of thermally-induced anemone bleaching on associated anemonefish hormonal stress response and reproduction. Nature Communications 8:1–9

  • Bellantuono AJ, Hoegh-Guldberg O, Rodriguez-Lanetty M (2011) Resistance to thermal stress in corals without changes in symbiont composition. Proceedings of the Royal Society B: Biological Sciences 279:1100–1107

  • Bindoff NL, Cheung WWL, Kairo JG, Arístegui J, Guinder VA, Hallberg R, Hilmi N, Jiao N, Karim MS, Levin LS, O’Donoghue S, Purca Cuicapusa SR, Rinkevich B, Suga T, Tagliabue A, Williamson P (2019) Changing Ocean, Marine Ecosystems, and Dependent Communities. In: Pörtner HO, Roberts DC, Masson-Delmotte V, Zhai P, Tignor M, Poloczanska E, Mintenbeck K, Alegría A, Nicolai M, Okem A, Petzold J, Rama A, Weyer NM (eds) IPCC Special Report on the Ocean and Cryosphere in a Changing Climate.

  • Brading P, Warner ME, Smith DJ, Suggett DJ (2013) Contrasting modes of inorganic carbon acquisition amongst Symbiodinium (Dinophyceae) phylotypes. New Phytologist 200:432–442

  • Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138

  • Brown KT, Bender-Champ D, Kenyon TM, Rémond C, Hoegh-Guldberg O, Dove S (2019) Temporal effects of ocean warming and acidification on coral–algal competition. Coral Reefs 38:297–309

  • Cleves PA, Krediet CJ, Lehnert EM, Onishi M, Pringle JR (2020) Insights into coral bleaching under heat stress from analysis of gene expression in a sea anemone model system. Proceedings of the National Academy of Sciences: 2015737117

  • Connell SD, Russell BD (2010) The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proceedings of the Royal Society B: Biological Sciences 277:1409–1415

  • Cox PM, Betts RA, Jones CD, Spall SA, Totterdell IJ (2000) Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408:184–187

  • Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiology and Molecular Biology Reviews 76:229–261

  • Dickson A, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Research Part A Oceanographic Research Papers 34:1733–1743

  • Duckworth AR, West L, Vansach T, Stubler A, Hardt M (2012) Effects of water temperature and pH on growth and metabolite biosynthesis of coral reef sponges. Marine Ecology Progress Series 462:67–77

  • Dunn D F (1981) The clownfish sea anemones: Stichodactylidae (Coelenterata: Actiniaria) and other sea anemones symbiotic with pomacentrid fishes. Transactions of the American Philosophical Society 71:3–115.

  • Duyens L (1956) The flattering of the absorption spectrum of suspensions, as compared to that of solutions. Biochimica et Biophysica Acta 19:1–12

  • Fautin DG, Allen GR (1992) Field guide to anemonefishes and their host sea anemones. Western Australian Museum, Perth, Australia

  • Fisher AC (2017) Climate change effects on photosynthetic symbionts in the sea anemone Anthopleura xanthogrammica. Doctoral dissertation, San Francisco State University

  • Furla P, Allemand D, Orsenigo M N (2000) Involvement of H-ATPase and carbonic anhydrase in inorganic carbon uptake for endosymbiont photosynthesis. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 278:870–881

  • Graham ER, Parekh A, Devassy RK, Sanders RW (2015) Carbonic anhydrase activity changes in response to increased temperature and pCO2 in Symbiodinium–zoanthid associations. Journal of Experimental Marine Biology and Ecology 473:218–226

  • Gibbin EM, Davy SK (2014) The photo-physiological response of a model cnidarian–dinoflagellate symbiosis to CO2- induced acidification at the cellular level. Journal of Experimental Marine Biology and Ecology 457:1–7

  • Godinot C, Houlbreque F, Grover R, Ferrier-Pagès C (2011) Coral uptake of inorganic phosphorus and nitrogen negatively affected by simultaneous changes in temperature and pH. PLoS One 6:e25024

  • Hagemeyer J (2016) Entering the Anthropocene: How ocean acidification and warmer temperatures affect the symbiotic sea anemone Exaiptasia pallida. Doctoral dissertation, University of Delaware

  • Hill R, Scott A (2012) The influence of irradiance on the severity of thermal bleaching in sea anemones that host anemonefish. Coral Reefs 31:273–284

  • Hawkins TD, Warner ME (2017) Warm preconditioning protects against acute heat-induced respiratory dysfunction and delays bleaching in a symbiotic sea anemone. Journal of Experimental Biology 220(6): 969–983

  • Hill R, Fernance C, Wilkinson SP, Davy SK, Scott A (2014) Symbiont shuffling during thermal bleaching and recovery in the sea anemone Entacmaea quadricolor. Marine Biology 161:2931–2937

  • Hoadley KD, Rollison D, Pettay DT, Warner ME (2015) Differential carbon utilisation and asexual reproduction under elevated pCO2 conditions in the model anemone, Exaiptasia pallida, hosting different symbionts. Limnology and Oceanography 60:2108–2120

  • Hobbs J-PA, Frisch AJ, Ford BM, Thums M, Saenz-Agudelo P, Furby KA, Berumen ML (2013) Taxonomic, spatial and temporal patterns of bleaching in anemones inhabited by anemonefishes. PLoS One 8:e70966

  • Hobday AJ, Lough JM (2011) Projected climate change in Australian marine and freshwater environments. Marine and Freshwater Research 62:1000–1014

  • Hobday AJ, Okey TA, Poloczanska ES, Kunz TJ, Richardson AJ (2006) Report to the Australian Greenhouse Office: Impacts of climate change on Australian marine life. Australian Greenhouse Office, in the Department of the Environment and Heritage Canberra, Australia

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research 50:839–866

  • Hoegh-Guldberg O, Smith GJ (1989) Influence of the population density of zooxanthellae and supply of ammonium on the biomass and metabolic characteristics of the reef corals Seriatopora hystrix and Stylophora pistillata. Marine Ecology Progress Series:173–186

  • Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328:1523–1528

  • Horvath KM, Castillo KD, Armstrong P, Westfield IT, Courtney T, Ries JB (2016) Next-century ocean acidification and warming both reduce calcification rate, but only acidification alters skeletal morphology of reef-building coral Siderastrea siderea. Scientific Reports 6:29613

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JB, Kleypas J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

  • Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377

  • Jeffrey S, Humphrey G (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochemie und Physiologie der Pflanzen 167:191–194

  • Jones A, Gardner S, Sinclair W (2008) Losing ‘Nemo’: bleaching and collection appear to reduce inshore populations of anemonefishes. Journal of Fish Biology 73:753–761

  • Jones RJ (1997) Changes in zooxanthellar densities and chlorophyll concentrations in corals during and after a bleaching event. Marine Ecology Progress Series 158:51–59

  • Jurriaans S, Hoogenboom MO (2019) Thermal performance of scleractinian corals along a latitudinal gradient on the Great Barrier Reef. Philosophical Transactions of the Royal Society B 374:20180546

  • Kelaher BP, Coleman MA, Bishop MJ (2018) Ocean warming, but not acidification, accelerates seagrass decomposition under near-future climate scenarios. Marine Ecology Progress Series 605:103–110

  • Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso JP (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Global Change Biology 19:1884–1896

  • Laurent J, Venn A, Tambutté É, Ganot P, Allemand D, Tambutté S (2014) Regulation of intracellular pH in cnidarians: response to acidosis in Anemonia viridis. The FEBS Journal 281:683–695

  • Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192’

  • Levin RA, Beltran VH, Hill R, Kjelleberg S, McDougald D, Steinberg PD, Van Oppen MJ (2016) Sex, scavengers, and chaperones: transcriptome secrets of divergent Symbiodinium thermal tolerances. Molecular Biology and Evolution 33:2201–2215

  • Lönnstedt OM, Frisch AJ (2014) Habitat bleaching disrupts threat responses and persistence in anemonefish. Marine Ecology Progress Series 517:265–270

  • Marshall NJ, Kleine DA, Dean AJ (2012) CoralWatch: education, monitoring, and sustainability through citizen science. Frontiers in Ecology and the Environment 10:332–334

  • Mason RA (2018) Decline in symbiont densities of tropical and subtropical scleractinian corals under ocean acidification. Coral Reefs 37:945–953

  • Matthews JL, Sproles AE, Oakley CA, Grossman AR, Weis VM, Davy SK (2016) Menthol-induced bleaching rapidly and effectively provides experimental aposymbiotic sea anemones (Aiptasia sp.) for symbiosis investigations. Journal of Experimental Biology 219(3): 306–310

  • Mehrbach C, Culberson CH, Hawley JE, Pytkowicx RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure 1. Limnology and Oceanography 18:897–907

  • Molina VH, Castillo-Medina RE, Thomé PE (2017) Experimentally induced bleaching in the Sea Anemone Exaiptasia supports glucose as a main metabolite associated with its symbiosis. Journal of Marine Biology 2017: 3130723

  • Moya A, Ganot P, Furla P, Sabourault C (2012) The transcriptomic response to thermal stress is immediate, transient and potentiated by ultraviolet radiation in the sea anemone Anemonia viridis. Molecular Ecology 21:1158–1174

  • Munday PL, Crawley NE, Nilsson GE (2009) Interacting effects of elevated temperature and ocean acidification on the aerobic performance of coral reef fishes. Marine Ecology Progress Series 388:235–242

  • Muscatine L, Falkowski P, Porter J, Dubinsky Z (1984) Fate of photosynthetic fixed carbon in light-and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proceedings of the Royal Society of London Series B Biological Sciences 222:181–202

  • Myhre G, Shindell D, Bréon F, Collins W, Fuglestvedt J, Huang J, Koch D, Lamarque J, Lee D, Mendoza B (2013) Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press Cambridge, New York, USA

  • Nakicenovic N, Alcamo J, Grubler A, Riahi K, Roehrl R, Rogner H-H, Victor N (2000) Special report on emissions scenarios (SRES), a special report of Working Group III of the intergovernmental panel on climate change. Cambridge University Press

  • Pêcheux M (2002) CO2 increase, a direct cause of coral reef mass bleaching. Marine Life 12:63–68

  • Perez SF, Cook CB, Brooks WR (2001) The role of symbiotic dinoflagellates in the temperature-induced bleaching response of the subtropical sea anemone Aiptasia pallida. Journal of Experimental Marine Biology and Ecology 256:1–14

  • Pierrot D, Lewis E, Wallace D (2006) CO2SYS DOS Program developed for CO2 system calculations. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, , Oak Ridge, USA

  • Pontasch S, Hill R, Deschaseaux E, Fisher P, Davy S, Scott A (2014a) Photochemical efficiency and antioxidant capacity in relation to Symbiodinium genotype and host phenotype in a symbiotic cnidarian. Marine Ecology Progress Series 516:195–208

  • Pontasch S, Scott A, Hill R, Bridge T, Fisher P, Davy S (2014b) Symbiodinium diversity in the sea anemone Entacmaea quadricolor on the east Australian coast. Coral Reefs 33:537–542

  • Pörtner H-O (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Marine Ecology Progress Series 373:203–218

  • Prada F, Caroselli E, Mengoli S, Brizi L, Fantazzini P, Capaccioni B, Pasquini L, Fabricius K, Dubinsky Z, Falini G (2017) Ocean warming and acidification synergistically increase coral mortality. Scientific Reports 7:40842

  • Reyes‐Nivia C, Diaz‐Pulido G, Kline D, Guldberg OH, Dove S (2013) Ocean acidification and warming scenarios increase microbioerosion of coral skeletons. Global Change Biology 19:1919–1929

  • Rodolfo-Metalpa R, Houlbrèque F, Tambutté É, Boisson F, Baggini C, Patti FP, Jeffree R, Fine M, Foggo A, Gattuso J (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nature Climate Change 1:308–312

  • Sadikot RT, Zeng H, Yull FE, Li B, Cheng D-s, Kernodle DS, Jansen ED, Contag CH, Segal BH, Holland SM (2004) p47phox deficiency impairs NF-κB activation and host defense in Pseudomonas pneumonia. The Journal of Immunology 172:1801–1808

  • Saenz-Agudelo P, Jones G, Thorrold S, Planes S (2011) Detrimental effects of host anemone bleaching on anemonefish populations. Coral Reefs 30:497–506

  • Scheufen T, Iglesias-Prieto R, Enríquez S (2017) Changes in the number of symbionts and Symbiodinium cell pigmentation modulate differentially coral light absorption and photosynthetic performance. Frontiers in Marine Science 4:309

  • Schoepf V, Grottoli AG, Warner ME, Cai W-J, Melman TF, Hoadley KD, Pettay DT, Hu X, Li Q, Xu H (2013) Coral energy reserves and calcification in a high-CO2 world at two temperatures. PloS one 8:e75049

  • Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou GC, Govindjee(eds) Chlorophyll a Fluorescence. Springer, Dordrecht, pp 279–319

  • Scott A, Hardefeldt JM, Hall KC (2014) Asexual propagation of sea anemones that host anemonefishes: implications for the marine ornamental aquarium trade and restocking programs. PLoS One 9(10):e109566

  • Scott A, Harrison P (2007) Broadcast spawning of two species of sea anemone, Entacmaea quadricolor and Heteractis crispa, that host anemonefish. Invertebrate Reproduction & Development 50:163–71

  • Scott A, Hoey AS (2017) Severe consequences for anemonefishes and their host sea anemones during the 2016 bleaching event at Lizard Island, Great Barrier Reef. Coral Reefs 36:873–873

  • Shenkar N, Fine M, Kramarsky-Winter E, Loya Y (2006) Population dynamics of zooxanthellae during a bacterial bleaching event. Coral Reefs 25:223–227

  • Siebeck U, Marshall N, Klüter A, Hoegh-Guldberg O (2006) Monitoring coral bleaching using a colour reference card. Coral Reefs 25:453–460

  • Suggett DJ, Hall‐Spencer JM, Rodolfo‐Metalpa R, Boatman TG, Payton R, Tye Pettay D, Johnson VR, Warner ME, Lawson T (2012) Sea anemones may thrive in a high CO2 world. Global Change Biology 18:3015–3025

  • Towanda T, Thuesen EV (2012) Prolonged exposure to elevated CO2 promotes growth of the algal symbiont Symbiodinium muscatinei in the intertidal sea anemone Anthopleura elegantissima. Biology Open 1:615–621

  • Ventura P, Jarrold MD, Merle PL, Barnay-Verdier S, Zamoum T, Rodolfo-Metalpa R, Calosi P, Furla P (2016) Resilience to ocean acidification: decreased carbonic anhydrase activity in sea anemones under high pCO2 conditions. Marine Ecology Progress Series 559:257–63

  • Weis VM (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. Journal of Experimental Biology 211:3059–3066

  • Weis VM, Reynolds WS (1999) Carbonic anhydrase expression and synthesis in the sea anemone Anthopleura elegantissima are enhanced by the presence of dinoflagellate symbionts. Physiological and Biochemical Zoology 72:307–316

  • Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant, Cell & Environment 31:679–694

  • Yuan X, Guo Y, Cai W, Huang H, Zhou W, Liu S (2019) Coral responses to ocean warming and acidification: Implications for future distribution of coral reefs in the South China Sea. Marine Pollution Bulletin 138:241–248

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Acknowledgements

We wish to thank Ceylena Holloway for help with sample processing, Bennan Chen, Damien Eggeling, Alison King, Kaycee Davis and Georgia Foley for technical support, Symon Dworjanyn for supplying equipment and Dive Quest and Matt Nimbs for helping collect sea anemones. Sea anemones were collected under NSW DPI Scientific Collection Permit (P02/0025-5.0). This study was funded by Sea World Research and Rescue Foundation Inc and Winifred Violet Scott Charitable Trust (SWR/4/2018).

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Pryor, S.H., Andrews, L., Kelaher, B.P. et al. Ocean temperature, but not acidification, causes sea anemone bleaching under a near-future climate scenario. Coral Reefs 40, 355–364 (2021). https://doi.org/10.1007/s00338-021-02050-9

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